Neuroprotective effects of the complement terminal pathway during demyelination: Implications for oligodendrocyte survival

Journal of Neuroimmunology

Volumn 213, Issue 1-2, 2009, Pages 3-11

  Tegla, Cosmin A ^a   Cudrici, Cornelia ^a   Rus, Violeta ^a   Ito, Takahiro ^a   Vlaicu, Sonia ^a   Singh, Anil ^a   Rus, Horea ^a,b  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Apoptosis; C5b 9 complement complex; Experimental allergic encephalomyelitis; Insulin like growth factor binding proteins; Multiple sclerosis; Oligodendrocyte

Indexed keywords

COMPLEMENT; COMPLEMENT COMPONENT C5B; COMPLEMENT COMPONENT C6; COMPLEMENT COMPONENT C7; COMPLEMENT COMPONENT C8; COMPLEMENT COMPONENT C9; FAS LIGAND; GAMMA INTERFERON; MYELIN; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND;

ALLERGIC ENCEPHALOMYELITIS; APOPTOSIS; CELL PROTECTION; CELL SURVIVAL; COMPLEMENT ACTIVATION; DEMYELINATION; EFFECTOR CELL; GLIOSIS; HUMAN; LYMPHOCYTE ACTIVATION; MACROPHAGE; MICROGLIA; MULTIPLE SCLEROSIS; NERVE FIBER; NEUROPROTECTION; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; PROTEIN ASSEMBLY; REMYELINIZATION; REVIEW;

ANIMALS; CELL SURVIVAL; COMPLEMENT MEMBRANE ATTACK COMPLEX; COMPLEMENT SYSTEM PROTEINS; CYTOPROTECTION; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; HUMANS; MULTIPLE SCLEROSIS; MYELIN SHEATH; OLIGODENDROGLIA; SIGNAL TRANSDUCTION;

EID: 68049129538     PISSN: 01655728     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jneuroim.2009.06.006     Document Type: Review

References (112)

1. Akassoglou K., Bauer J., Kassiotis G., Pasparakis M., Lassmann H., Kollias G., and Probert L. Oligodendrocyte apoptosis and primary demyelination induced by local TNF/p55TNF receptor signaling in the central nervous system of transgenic mice: models for multiple sclerosis with primary oligodendrogliopathy. Am. J. Pathol. 153 (1998) 801-813
2. Alberdi E., Sanchez-Gomez M.V., Torre I., Domercq M., Perez-Samartin A., Perez-Cerda F., and Matute C. Activation of kainate receptors sensitizes oligodendrocytes to complement attack. J. Neurosci. 26 (2006) 3220-3228
3. Andrews T., Zhang P., and Bhat N.R. TNFalpha potentiates IFNgamma-induced cell death in oligodendrocyte progenitors. J. Neurosci. Res. 54 (1998) 574-583
4. Antel J.P., McCrea E., Ladiwala U., Qin Y.F., and Becher B. Non-MHC-restricted cell-mediated lysis of human oligodendrocytes in vitro: relation with CD56 expression. J. Immunol. 160 (1998) 1606-1611
5. Ashburner M., Ball C.A., Blake J.A., Botstein D., Butler H., Cherry J.M., Davis A.P., Dolinski K., Dwight S.S., Eppig J.T., Harris M.A., Hill D.P., Issel-Tarver L., Kasarskis A., Lewis S., Matese J.C., Richardson J.E., Ringwald M., Rubin G.M., and Sherlock G. Gene ontology: tool for the unification of biology. Gene Ontol. Consortium. Nat. Genet. 25 (2000) 25-29
6. Bailey S.L., Schreiner B., McMahon E.J., and Miller S.D. CNS myeloid DCs presenting endogenous myelin peptides 'preferentially' polarize CD4+ T(H)-17 cells in relapsing EAE. Nat. Immunol. 8 (2007) 172-180
7. Barnett M.H., and Prineas J.W. Relapsing and remitting multiple sclerosis: pathology of the newly forming lesion. Ann. Neurol. 55 (2004) 458-468
8. Barnett M.H., Parratt J.D., Cho E.S., and Prineas J.W. Immunoglobulins and complement in postmortem multiple sclerosis tissue. Ann. Neurol. 65 (2009) 32-46
9. Beattie M.S., Harrington A.W., Lee R., Kim J.Y., Boyce S.L., Longo F.M., Bresnahan J.C., Hempstead B.L., and Yoon S.O. ProNGF induces p75-mediated death of oligodendrocytes following spinal cord injury. Neuron 36 (2002) 375-386
10. Blink S.E., and Miller S.D. The contribution of gammadelta T cells to the pathogenesis of EAE and MS. Curr. Mol. Med. 9 (2009) 15-22
11. Bonetti B., and Raine C.S. Multiple sclerosis: oligodendrocytes display cell death-related molecules in situ but do not undergo apoptosis. Ann. Neurol. 42 (1997) 74-84
12. Breij E.C.W., Brink B.P., Veerhuis R., Van den Berg C., Vloet R., Yan R., Dijkstra C.D., Van der Valk P., and Bö L. Homogeneity of active demyelinating lesions in established multiple sclerosis. Ann. Neurol. 63 (2008) 16-25
13. Brink B.P., Veerhuis R., Breij E.C., van der Valk P., Dijkstra C.D., and Bo L. The pathology of multiple sclerosis is location-dependent: no significant complement activation is detected in purely cortical lesions. J. Neuropathol. Exp. Neurol. 64 (2005) 147-155
14. Cannella B., Gaupp S., Omari K.M., and Raine C.S. Multiple sclerosis: death receptor expression and oligodendrocyte apoptosis in established lesions. J. Neuroimmunol. 188 (2007) 128-137
15. Casaccia-Bonnefil P., Carter B.D., Dobrowsky R.T., and Chao M.V. Death of oligodendrocytes mediated by the interaction of nerve growth factor with its receptor p75. Nature 383 (1996) 716-719
16. Chavez-Galan L., Arenas-Del Angel M.C., Zenteno E., Chavez R., and Lascurain R. Cell death mechanisms induced by cytotoxic lymphocytes. Cell Mol. Immunol. 6 (2009) 15-25
17. Choi C., and Benveniste E.N. Fas ligand/Fas system in the brain: regulator of immune and apoptotic responses. Brain Res. Brain Res. Rev. 44 (2004) 65-81
18. Comabella M., and Martin R. Genomics in multiple sclerosis-current state and future directions. J. Neuroimmunol. 187 (2007) 1-8
19. Compston D.A., Morgan B.P., Campbell A.K., Wilkins P., Cole G., Thomas N.D., and Jasani B. Immunocytochemical localization of the terminal complement complex in multiple sclerosis. Neuropathol. Appl. Neurobiol. 15 (1989) 307-316
20. Cudrici C., Summers D., Jansen T., Fosbrink M., and Rus H. C5b-9 protects oligodendrocytes apoptosis by regulating BH-3-only proapoptotic proteins. FASEB J. 19 (2005) A324
21. Cudrici C., Niculescu F., Jensen T., Zafranskaia E., Fosbrink M., Rus V., Shin M.L., and Rus H. C5b-9 terminal complex protects oligodendrocytes from apoptotic cell death by inhibiting caspase-8 processing and up-regulating FLIP. J. Immunol. 176 (2006) 3173-3180
22. Cudrici C., Ito T., Zafranskaia E., Weerth S., Rus V., Chen H., Niculescu F., Soloviova K., Tegla C., Gherman A., Raine C.S., Shin M.L., and Rus H. Complement C5 regulates the expression of insulin-like growth factor binding proteins in chronic experimental allergic encephalomyelitis. J. Neuroimmunol. 203 (2008) 94-103
23. D'Souza S.D., Bonetti B., Balasingam V., Cashman N.R., Barker P.A., Troutt A.B., Raine C.S., and Antel J.P. Multiple sclerosis: Fas signaling in oligodendrocyte cell death. J. Exp. Med. 184 (1996) 2361-2370
24. Dowling P., Shang G., Raval S., Menonna J., Cook S., and Husar W. Involvement of the CD59 (APO-1/Fas) receptor ligand system in multiple sclerosis brain. J. Exp. Med. 184 (1996) 1315-1318
25. Dowling P., Husar W., Menonna J., Donnenfeld H., Cook S., and Sidhu M. Cell death and birth in multiple sclerosis brain. J. Neurol. Sci. 149 (1997) 1-11
26. Ewings K.E., Hadfield-Moorhouse K., Wiggins C.M., Wickenden J.A., Balmanno K., Gilley R., Degenhardt K., White E., and Cook S.J. ERK1/2-dependent phosphorylation of BimEL promotes its rapid dissociation from Mcl-1 and Bcl-xL. Embo. J. 26 (2007) 2856-2867
27. Frank M.M., and Atkinson J.P. Complement system. In: Austen K.F., Frank M.M., Atkinson J.P., and Cantor H. (Eds). Samter's Immunologic Diseases (2001), Lippincott Williams & Wilkins, Boston 281-298
28. Frohman E.M., Racke M.K., and Raine C.S. Multiple sclerosis-the plaque and its pathogenesis. N. Engl. J. Med. 354 (2006) 942-955
29. Furlan R., Martino G., Galbiati F., Poliani P.L., Smiroldo S., Bergami A., Desina G., Comi G., Flavell R., Su M.S., and Adorini L. Caspase-1 regulates the inflammatory process leading to autoimmune demyelination. J. Immunol. 163 (1999) 2403-2409
30. Gonzalvez F., Schug Z.T., Houtkooper R.H., MacKenzie E.D., Brooks D.G., Wanders R.J.A., Petit P.X., Vaz F.M., and Gottlieb E. Cardiolipin provides an essential activating platform for caspase-8 on mitochondria. J. Biol. Chem. 183 (2008) 681-696
31. Gveric D., Cuzner M.L., and Newcombe J. Insulin-like growth factors and binding proteins in multiple sclerosis plaques. Neuropathol. Appl. Neurobiol. 25 (1999) 215-225
32. Harrison D.C., Roberts* J., Campbell C.A., Crook B., Davis R., Deen K., Meakin J., Michalovich D., Price J., Stammers M., and Maycox P.R. TR3 death receptor expression in the normal and ischaemic brain. Neuroscience 96 (2000) 147-160
33. Heppner F.L., Greter M., Marino D., Falsig J., Raivich G., Hovelmeyer N., Waisman A., Rulicke T., Prinz M., Priller J., Becher B., and Aguzzi A. Experimental autoimmune encephalomyelitis repressed by microglial paralysis. Nat. Med. 11 (2005) 146-152
34. Hestvik A.L., Skorstad G., Vartdal F., and Holmoy T. Idiotope-specific CD4(+) T cells induce apoptosis of human oligodendrocytes. J. Autoimmun. 32 (2009) 125-132
35. Hisahara S., Shoji S., Okano H., and Miura M. ICE/CED-3 family executes oligodendrocyte apoptosis by tumor necrosis factor. J. Neurochem. 69 (1997) 10-20
36. Hisahara S., Araki T., Sugiyama F., Yagami K., Suzuki M., Abe K., Yamamura K., Miyazaki J., Momoi T., Saruta T., Bernard C.C., Okano H., and Miura M. Targeted expression of baculovirus p35 caspase inhibitor in oligodendrocytes protects mice against autoimmune-mediated demyelination. Embo. J. 19 (2000) 341-348
37. Hisahara S., Yuan J., Momoi T., Okano H., and Miura M. Caspase-11 mediates oligodendrocyte cell death and pathogenesis of autoimmune-mediated demyelination. J. Exp. Med. 193 (2001) 111-122
38. Holley J.E., Gveric D., Newcombe J., Cuzner M.L., and Gutowski N.J. Astrocyte characterization in the multiple sclerosis glial scar. Neuropathol. Appl. Neurobiol. 29 (2003) 434-444
39. Hosack D.A., Dennis Jr. G., Sherman B.T., Lane H.C., and Lempicki R.A. Identifying biological themes within lists of genes with EASE. Genome. Biol. 4 (2003) R70
40. Iacobas D.A., Iacobas S., Werner P., Scemes E., and Spray D.C. Alteration of transcriptomic networks in adoptive-transfer experimental autoimmune encephalomyelitis. Front. Integr. Neurosci. 1 (2007) 10
41. Jack C., Antel J., Bruck W., and Kuhlmann T. Contrasting potential of nitric oxide and peroxynitrite to mediate oligodendrocyte injury in multiple sclerosis. Glia 55 (2007) 926-934
42. Jana A., and Pahan K. Oxidative stress kills human primary oligodendrocytes via neutral sphingomyelinase: implications for multiple sclerosis. J. Neuroimmune. Pharmacol. 2 (2007) 184-193
43. John G.R., Shankar S.L., Shafit-Zagardo B., Massimi A., Lee S.C., Raine C.S., and Brosnan C.F. Multiple sclerosis: re-expression of a developmental pathway that restricts oligodendrocyte maturation. Nat. Med. 8 (2002) 1115-1121
44. Jurewicz A., Biddison W.E., and Antel J.P. MHC class I-restricted lysis of human oligodendrocytes by myelin basic protein peptide-specific CD8 T lymphocytes. J. Immunol. 160 (1998) 3056-3059
45. Jurewicz A., Matysiak M., Tybor K., and Selmaj K. TNF-induced death of adult human oligodendrocytes is mediated by c-jun NH2-terminal kinase-3. Brain 126 (2003) 1358-1370
46. Jurewicz A., Matysiak M., Tybor K., Kilianek L., Raine C.S., and Selmaj K. Tumour necrosis factor-induced death of adult human oligodendrocytes is mediated by apoptosis inducing factor. Brain 128 (2005) 2675-2688
47. Jurewicz A., Matysiak M., Andrzejak S., and Selmaj K. TRAIL-induced death of human adult oligodendrocytes is mediated by JNK pathway. Glia 53 (2006) 158-166
48. Khurana R., Zhuang Z., Bhardwaj S., Murakami M., De Muinck E., Yla-Herttuala S., Ferrara N., Martin J.F., Zachary I., and Simons M. Angiogenesis-dependent and independent phases of intimal hyperplasia. Circulation 110 (2004) 2436-2443
49. Koski C.L., Ramm L.E., Hammer C.H., Mayer M.M., and Shin M.L. Cytolysis of nucleated cells by complement: cell death displays multi-hit characteristics. Proc. Natl. Acad. Sci. U. S. A. 80 (1983) 3816-3820
50. Kuhlmann T., Miron V., Cuo Q., Wegner C., Antel J., and Bruck W. Differentiation block of oligodendroglial progenitor cells as a cause for remyelination failure in chronic multiple sclerosis. Brain 131 (2008) 1749-1758
51. Lassmann H., Brück W., and Lucchinetti C. The immunopathology of multiple sclerosis: an overview. Brain Pathol. 17 (2007) 210-218
52. Lavrik I.N., Golks A., and Krammer P.H. Caspases: pharmacological manipulation of cell death. J. Clin. Invest. 115 (2005) 2665-2672
53. Li W., Maeda Y., Ming X., Cook S., Chapin J., Husar W., and Dowling P. Apoptotic death following Fas activation in human oligodendrocyte hybrid cultures. J. Neurosci. Res. 69 (2002) 189-196
54. Lin W., Harding H.P., Ron D., and Popko B. Endoplasmic reticulum stress modulates the response of myelinating oligodendrocytes to the immune cytokine interferon-{gamma}. J. Cell Biol. 169 (2005) 603-612
55. Lin W., Kemper A., Dupree J.L., Harding H.P., Ron D., and Popko B. Interferon-{gamma} inhibits central nervous system remyelination through a process modulated by endoplasmic reticulum stress. Brain 129 (2006) 1306-1318
56. Liu W.T., Vanguri P., and Shin M.L. Studies on demyelination in vitro: the requirement of membrane attack components of the complement system. J. Immunol. 131 (1983) 778-782
57. Louis J.C., Magal E., Takayama S., and Varon S. CNTF protection of oligodendrocytes against natural and tumor necrosis factor-induced death. Science 259 (1993) 689-692
58. Lucchinetti C., Bruck W., Parisi J., Scheithauer B., Rodriguez M., and Lassmann H. Heterogeneity of multiple sclerosis lesions: implications for the pathogenesis of demyelination. Ann. Neurol. 47 (2000) 707-717
59. Lucchinetti C.F., Mandler R.N., McGavern D., Bruck W., Gleich G., Ransohoff R.M., Trebst C., Weinshenker B., Wingerchuk D., Parisi J.E., and Lassmann H. A role for humoral mechanisms in the pathogenesis of Devic's neuromyelitis optica. Brain 125 (2002) 1450-1461
60. Matute C., Sanchez-Gomez M.V., Martinez-Millan L., and Miledi R. Glutamate receptor-mediated toxicity in optic nerve oligodendrocytes. Proc. Natl. Acad. Sci. U. S. A. 94 (1997) 8830-8835
61. Matysiak M., Jurewicz A., Jaskolski D., and Selmaj K. TRAIL induces death of human oligodendrocytes isolated from adult brain 125 (2002) 2469-2480
62. Merrill J.E., Ignarro L.J., Sherman M.P., Melinek J., and Lane T.E. Microglial cell cytotoxicity of oligodendrocytes is mediated through nitric oxide. J. Immunol. 151 (1993) 2132-2141
63. Ming X., Li W., Maeda Y., Blumberg B., Raval S., Cook S.D., and Dowling P.C. Caspase-1 expression in multiple sclerosis plaques and cultured glial cells. J. Neurol. Sci. 197 (2002) 9-18
64. Mohan N., Edwards E.T., Cupps T.R., Oliverio P.J., Sandberg G., Crayton H., Richert J.R., and Siegel J.N. Demyelination occurring during anti-tumor necrosis factor alpha therapy for inflammatory arthritides. Arthritis. Rheum. 44 (2001) 2862-2869
65. Mollnes T.E., Vandvik B., Lea T., and Vartdal F. Intrathecal complement activation in neurological diseases evaluated by analysis of the terminal complement complex. J. Neurol. Sci. 78 (1987) 17-28
66. Morse R.H., Seguin R., McCrea E.L., and Antel J.P. NK cell-mediated lysis of autologous human oligodendrocytes. J. Neuroimmunol. 116 (2001) 107-115
67. Niculescu F., and Rus H. Mechanisms of signal transduction activated by sublytic assembly of terminal complement complexes on nucleated cells. Immunol. Res. 24 (2001) 191-199
68. Niculescu T., Weerth S., Niculescu F., Cudrici C., Rus V., Raine C.S., Shin M.L., and Rus H. Effects of complement C5 on apoptosis in experimental autoimmune encephalomyelitis. J. Immunol. 172 (2004) 5702-5706
69. Ousman S.S., Tomooka B.H., van Noort J.M., Wawrousek E.F., O/'Conner K., Hafler D.A., Sobel R.A., Robinson W.H., and Steinman L. Protective and therapeutic role for [alpha]B-crystallin in autoimmune demyelination. Nature 448 (2007) 474-479
70. Ozawa K., Suchanek G., Breitschopf H., Bruck W., Budka H., Jellinger K., and Lassmann H. Patterns of oligodendroglia pathology in multiple sclerosis. Brain 117 Pt 6 (1994) 1311-1322
71. Panitch H.S., Hirsch R.L., Schindler J., and Johnson K.P. Treatment of multiple sclerosis with gamma interferon: exacerbations associated with activation of the immune system. Neurology 37 (1987) 1097-1102
72. Pitt D., Werner P., and Raine C.S. Glutamate excitotoxicity in a model of multiple sclerosis. Nat. Med. 6 (2000) 67-70
73. Pouly S., Becher B., Blain M., and Antel J.P. Interferon-gamma modulates human oligodendrocyte susceptibility to Fas-mediated apoptosis. J. Neuropathol. Exp. Neurol. 59 (2000) 280-286
74. Prineas J.W., Kwon E.E., Cho E.S., Sharer L.R., Barnett M.H., Oleszak E.L., Hoffman B., and Morgan B.P. Immunopathology of secondary-progressive multiple sclerosis. Ann. Neurol. 50 (2001) 646-657
75. Raine C. Multiple sclerosis: classification revisited reveals homogeneity and recapitulation. Ann. Neurol. 63 (2008) 1-3
76. Reiman R., Gerard C., Campbell I.L., and Barnum S.R. Disruption of the C5a receptor gene fails to protect against experimental allergic encephalomyelitis. Eur. J. Immunol. 32 (2002) 1157-1163
77. Robbins D.S., Shirazi Y., Drysdale B.E., Lieberman A., Shin H.S., and Shin M.L. Production of cytotoxic factor for oligodendrocytes by stimulated astrocytes. J. Immunol. 139 (1987) 2593-2597
78. Ruijs T.C., Louste K., Brown E.A., and Antel J.P. Lysis of human glial cells by major histocompatibility complex-unrestricted CD4+ cytotoxic lymphocytes. J. Neuroimmunol. 42 (1993) 105-111
79. Rus H.G., Niculescu F., and Shin M.L. Sublytic complement attack induces cell cycle in oligodendrocytes. J. Immunol. 156 (1996) 4892-4900
80. Rus H., Cudrici C., David S., and Niculescu F. The complement system in central nervous system diseases. Autoimmunity 39 (2006) 395-402
81. Saikali P., Antel J.P., Newcombe J., Chen Z., Freedman M., Blain M., Cayrol R., Prat A., Hall J.A., and Arbour N. NKG2D-mediated cytotoxicity toward oligodendrocytes suggests a mechanism for tissue injury in multiple sclerosis. J. Neurosci. 27 (2007) 1220-1228
82. Sanchez-Gomez M.V., Alberdi E., Ibarretxe G., Torre I., and Matute C. Caspase-dependent and caspase-independent oligodendrocyte death mediated by AMPA and kainate receptors. J. Neurosci. 23 (2003) 9519-9528
83. Sanders M.E., Alexander E.L., Koski C.L., Shin M.L., Sano Y., Frank M.M., and Joiner K.A. Terminal complement complexes (SC5b-9) in cerebrospinal fluid in autoimmune nervous system diseases. Ann. N. Y. Acad. Sci. 540 (1988) 387-388
84. Saxena A., Bauer J., Scheikl T., Zappulla J., Audebert M., Desbois S., Waisman A., Lassmann H., Liblau R.S., and Mars L.T. Cutting edge: multiple sclerosis-like lesions induced by effector CD8 T cells recognizing a sequestered antigen on oligodendrocytes. J. Immunol. 181 (2008) 1617-1621
85. Scolding N.J., Morgan B.P., Houston W.A., Linington C., Campbell A.K., and Compston D.A. Vesicular removal by oligodendrocytes of membrane attack complexes formed by activated complement. Nature 339 (1989) 620-622
86. Scolding N.J., Jones J., Compston D.A., and Morgan B.P. Oligodendrocyte susceptibility to injury by T-cell perforin. Immunology 70 (1990) 6-10
87. Seil F.J. Tissue culture studies of demyelinating disease: a critical review. Ann. Neurol. 2 (1977) 345-355
88. Sellebjerg F., Jaliashvili I., Christiansen M., and Garred P. Intrathecal activation of the complement system and disability in multiple sclerosis. J. Neurol. Sci. 157 (1998) 168-174
89. Selmaj K.W., and Raine C.S. Tumor necrosis factor mediates myelin and oligodendrocyte damage in vitro. Ann. Neurol. 23 (1988) 339-346
90. Selmaj K., Brosnan C.F., and Raine C.S. Colocalization of lymphocytes bearing gamma delta T-cell receptor and heat shock protein hsp65+ oligodendrocytes in multiple sclerosis. Proc. Natl. Acad. Sci. U. S. A. 88 (1991) 6452-6456
91. Selmaj K., Raine C.S., Farooq M., Norton W.T., and Brosnan C.F. Cytokine cytotoxicity against oligodendrocytes. Apoptosis. induced. by. lymphotoxin. J. Immunol. 147 (1991) 1522-1529
92. Sharief M.K., and Hentges R. Association between tumor necrosis factor-alpha and disease progression in patients with multiple sclerosis. N. Engl. J. Med. 325 (1991) 467-472
93. Sharma K., Wang R.X., Zhang L.Y., Yin D.L., Luo X.Y., Solomon J.C., Jiang R.F., Markos K., Davidson W., Scott D.W., and Shi Y.F. Death the Fas way: regulation and pathophysiology of CD95 and its ligand. Pharmacol. Ther. 88 (2000) 333-347
94. Shin M.L., Rus H.G., and Niculescu F.I. Membranes attack by complement: assembly and biology of the terminal complement complexes. In: Lee A. (Ed). Biomembranes 4 (1996), JAI Press, Greenwich, CT 123-149
95. Smith T., Groom A., Zhu B., and Turski L. Autoimmune encephalomyelitis ameliorated by AMPA antagonists. Nat. Med. 6 (2000) 62-66
96. Soane L., Rus H., Niculescu F., and Shin M.L. Inhibition of oligodendrocyte apoptosis by sublytic C5b-9 is associated with enhanced synthesis of bcl-2 and mediated by inhibition of caspase-3 activation. J. Immunol. 163 (1999) 6132-6138
97. Soane L., Cho H.J., Niculescu F., Rus H., and Shin M.L. C5b-9 terminal complement complex protects oligodendrocytes from death by regulating Bad through phosphatidylinositol 3-kinase/Akt pathway. J. Immunol. 167 (2001) 2305-2311
98. Storch M.K., Piddlesden S., Haltia M., Iivanainen M., Morgan P., and Lassmann H. Multiple sclerosis: in situ evidence for antibody- and complement-mediated demyelination. Ann. Neurol. 43 (1998) 465-471
99. Traugott U., and Raine C.S. Further lymphocyte characterization in the central nervous system in multiple sclerosis. Ann. N. Y. Acad. Sci. 436 (1984) 163-180
100. Vartanian T., Li Y., Zhao M., and Stefansson K. Interferon-gamma-induced oligodendrocyte cell death: implications for the pathogenesis of multiple sclerosis. Mol. Med. 1 (1995) 732-743
101. Walport M.J. Complement. First of two parts. N. Engl. J. Med. 344 (2001) 1058-1066
102. Weerth S.H., Rus H., Shin M.L., and Raine C.S. Complement C5 in experimental autoimmune encephalomyelitis (EAE) facilitates remyelination and prevents gliosis. Am. J. Pathol. 163 (2003) 1069-1080
103. Werner P., Pitt D., and Raine C.S. Multiple sclerosis: altered glutamate homeostasis in lesions correlates with oligodendrocyte and axonal damage. Ann. Neurol. 50 (2001) 169-180
104. Wilczak N., Chesik D., Hoekstra D., and De Keyser J. IGF binding protein alterations on periplaque oligodendrocytes in multiple sclerosis: Implications for remyelination. Neurochem. Int. 52 (2008) 1431-1435
105. Willis S.N., and Adams J.M. Life in the balance: how BH3-only proteins induce apoptosis. Curr. Opin. Cell Biol. 17 (2005) 617-625
106. Wolswijk G. Oligodendrocyte survival, loss and birth in lesions of chronic-stage multiple sclerosis. Brain 123 Pt 1 (2000) 105-115
107. Wosik K., Antel J., Kuhlmann T., Brück W., Massie B., and Nalbantoglu J. Oligodendrocyte injury in multiple sclerosis: a role for p53. J. Neurochem. 85 (2003) 635-644
108. Wosik K., Ruffini F., Almazan G., Olivier A., Nalbantoglu J., and Antel J.P. Resistance of human adult oligodendrocytes to AMPA/kainate receptor-mediated glutamate injury. Brain 127 (2004) 2636-2648
109. Wren D.R., and Noble M. Oligodendrocytes and oligodendrocyte/type-2 astrocyte progenitor cells of adult rats are specifically susceptible to the lytic effects of complement in absence of antibody. Proc. Natl. Acad. Sci. U. S. A. 86 (1989) 9025-9029
110. Wucherpfennig K.W., Newcombe J., Li H., Keddy C., Cuzner M.L., and Hafler D.A. Gamma delta T-cell receptor repertoire in acute multiple sclerosis lesions. Proc. Natl. Acad. Sci. U. S. A. 89 (1992) 4588-4592
111. Zeine R., Pon R., Ladiwala U., Antel J.P., Filion L.G., and Freedman M.S. Mechanism of gammadelta T cell-induced human oligodendrocyte cytotoxicity: relevance to multiple sclerosis. J. Neuroimmunol. 87 (1998) 49-61
112. Zeine R., Cammer W., Barbarese E., Liu C.C., and Raine C.S. Structural dynamics of oligodendrocyte lysis by perforin in culture: relevance to multiple sclerosis. J. Neurosci. Res. 64 (2001) 380-391